Intra-tumor Genetic Heterogeneity and Mortality in Head and Neck Cancer: Analysis of Data from The Cancer Genome Atlas

1. Hakansson L, Trope C (1974) On the presence within tumours of clones that differ in sensitivity to cytostatic drugs. Acta Pathol Microbiol Scand A 82: 35–40. 4827349

2. Nowell PC (1976) The clonal evolution of tumor cell populations. Science 194: 23–28. 959840

3. Fidler IJ, Kripke ML (1977) Metastasis results from preexisting variant cells within a malignant tumor. Science 197: 893–895. 887927

4. Dexter DL, Kowalski HM, Blazar BA, Fligiel Z, Vogel R, et al. (1978) Heterogeneity of tumor cells from a single mouse mammary tumor. Cancer Res 38: 3174–3181. 210930

5. Heppner GH (1984) Tumor heterogeneity. Cancer Res 44: 2259–2265. 6372991

6. Almendro V, Marusyk A, Polyak K (2013) Cellular heterogeneity and molecular evolution in cancer. Annu Rev Pathol 8: 277–302. doi: 10.1146/annurev-pathol-020712-163923 23092187

7. Burrell RA, McGranahan N, Bartek J, Swanton C (2013) The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501: 338–345. doi: 10.1038/nature12625 24048066

8. Bedard PL, Hansen AR, Ratain MJ, Siu LL (2013) Tumour heterogeneity in the clinic. Nature 501: 355–364. doi: 10.1038/nature12627 24048068

9. Gerashchenko TS, Denisov EV, Litviakov NV, Zavyalova MV, Vtorushin SV, et al. (2013) Intratumor heterogeneity: nature and biological significance. Biochemistry (Mosc) 78: 1201–1215. doi: 10.1134/S0006297913110011 24460935

10. Murugaesu N, Chew SK, Swanton C (2013) Adapting clinical paradigms to the challenges of cancer clonal evolution. Am J Pathol 182: 1962–1971. doi: 10.1016/j.ajpath.2013.02.026 23708210

11. Hiley C, de Bruin EC, McGranahan N, Swanton C (2014) Deciphering intratumor heterogeneity and temporal acquisition of driver events to refine precision medicine. Genome Biol 15: 453. doi: 10.1186/s13059-014-0453-8 25222836

12. Ciriello G, Miller ML, Aksoy BA, Senbabaoglu Y, Schultz N, et al. (2013) Emerging landscape of oncogenic signatures across human cancers. Nat Genet 45: 1127–1133. doi: 10.1038/ng.2762 24071851

13. Cooke SL, Temple J, Macarthur S, Zahra MA, Tan LT, et al. (2011) Intra-tumour genetic heterogeneity and poor chemoradiotherapy response in cervical cancer. Br J Cancer 104: 361–368. doi: 10.1038/sj.bjc.6605971 21063398

14. Gerlinger M, Horswell S, Larkin J, Rowan AJ, Salm MP, et al. (2014) Genomic architecture and evolution of clear cell renal cell carcinomas defined by multiregion sequencing. Nat Genet 46: 225–233. doi: 10.1038/ng.2891 24487277

15. Salvati F, Teodori L, Gagliardi L, Signora M, Aquilini M, et al. (1989) DNA flow cytometric studies of 66 human lung tumors analyzed before treatment. Prognostic implications. Chest 96: 1092–1098. 2553342

16. Millot C, Dufer J (2000) Clinical applications of image cytometry to human tumour analysis. Histol Histopathol 15: 1185–1200. 11005244

17. Park SY, Gonen M, Kim HJ, Michor F, Polyak K (2010) Cellular and genetic diversity in the progression of in situ human breast carcinomas to an invasive phenotype. J Clin Invest 120: 636–644. doi: 10.1172/JCI40724 20101094

18. Snuderl M, Fazlollahi L, Le LP, Nitta M, Zhelyazkova BH, et al. (2011) Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 20: 810–817. doi: 10.1016/j.ccr.2011.11.005 22137795

19. Maley CC, Galipeau PC, Finley JC, Wongsurawat VJ, Li X, et al. (2006) Genetic clonal diversity predicts progression to esophageal adenocarcinoma. Nat Genet 38: 468–473. 16565718

20. Navin N, Kendall J, Troge J, Andrews P, Rodgers L, et al. (2011) Tumour evolution inferred by single-cell sequencing. Nature 472: 90–94. doi: 10.1038/nature09807 21399628

21. Shah SP, Roth A, Goya R, Oloumi A, Ha G, et al. (2012) The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature 486: 395–399. doi: 10.1038/nature10933 22495314

22. Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, et al. (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366: 883–892. doi: 10.1056/NEJMoa1113205 22397650

23. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, et al., editors (2010) AJCC cancer staging manual, 7th ed. New York: Springer. 648 p.

24. Ding L, Raphael BJ, Chen F, Wendl MC (2013) Advances for studying clonal evolution in cancer. Cancer Lett 340: 212–219. doi: 10.1016/j.canlet.2012.12.028 23353056

25. Patel AP, Tirosh I, Trombetta JJ, Shalek AK, Gillespie SM, et al. (2014) Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 344: 1396–1401. doi: 10.1126/science.1254257 24925914

26. Carter SL, Cibulskis K, Helman E, McKenna A, Shen H, et al. (2012) Absolute quantification of somatic DNA alterations in human cancer. Nat Biotechnol 30: 413–421. doi: 10.1038/nbt.2203 22544022

27. Andor N, Harness JV, Muller S, Mewes HW, Petritsch C (2014) EXPANDS: expanding ploidy and allele frequency on nested subpopulations. Bioinformatics 30: 50–60. doi: 10.1093/bioinformatics/btt622 24177718

28. Oesper L, Satas G, Raphael BJ (2014) Quantifying tumor heterogeneity in whole-genome and whole-exome sequencing data. Bioinformatics 30: 3532–3540. doi: 10.1093/bioinformatics/btu651 25297070

29. Lonnstedt IM, Caramia F, Li J, Fumagalli D, Salgado R, et al. (2014) Deciphering clonality in aneuploid tumors using SNP array and sequencing data. Genome Biol 15: 470. doi: 10.1186/s13059-014-0470-7 25270265

30. Mroz EA, Rocco JW (2013) MATH, a novel measure of intratumor genetic heterogeneity, is high in poor-outcome classes of head and neck squamous cell carcinoma. Oral Oncol 49: 211–215. doi: 10.1016/j.oraloncology.2012.09.007 23079694

31. Mroz EA, Tward AD, Pickering CR, Myers JN, Ferris RL, et al. (2013) High intratumor genetic heterogeneity is related to worse outcome in patients with head and neck squamous cell carcinoma. Cancer 119: 3034–3042. doi: 10.1002/cncr.28150 23696076

32. Biesecker LG, Burke W, Kohane I, Plon SE, Zimmern R (2012) Next-generation sequencing in the clinic: are we ready? Nat Rev Genet 13: 818–824. doi: 10.1038/nrg3357 23076269

33. Stransky N, Egloff AM, Tward AD, Kostic AD, Cibulskis K, et al. (2011) The mutational landscape of head and neck squamous cell carcinoma. Science 333: 1157–1160. doi: 10.1126/science.1208130 21798893

34. Fakhry C, Westra WH, Li S, Cmelak A, Ridge JA, et al. (2008) Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst 100: 261–269. doi: 10.1093/jnci/djn011 18270337

35. Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, et al. (2011) Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 29: 4294–4301. doi: 10.1200/JCO.2011.36.4596 21969503

36. Bonilla-Velez J, Mroz EA, Hammon RJ, Rocco JW (2013) Impact of human papillomavirus on oropharyngeal cancer biology and response to therapy: implications for treatment. Otolaryngol Clin North Am 46: 521–543. doi: 10.1016/j.otc.2013.04.009 23910468

37. The Cancer Genome Atlas Research Network, Weinstein JN, Collisson EA, Mills GB, Shaw KR, et al. (2013) The Cancer Genome Atlas Pan-Cancer analysis project. Nat Genet 45: 1113–1120. doi: 10.1038/ng.2764 24071849

38. Poeta ML, Manola J, Goldwasser MA, Forastiere A, Benoit N, et al. (2007) TP53 mutations and survival in squamous-cell carcinoma of the head and neck. N Engl J Med 357: 2552–2561. 18094376

39. The Cancer Genome Atlas (2015) Data Matrix datasets: HNSC Data Matrix [database]. Available: https://tcga-data.nci.nih.gov/tcga/dataAccessMatrix.htm?mode=ApplyFilter&showMatrix=true&diseaseType=HNSC&tumorNormal=TN&tumorNormal=T&tumorNormal=NT&platformType=-999. Accessed 8 January 2015.

40. Hayes N (2012) Comprehensive genomic characterization of squamous cell carcinoma of the head and neck. Available: http://www.genome.gov/Multimedia/Slides/TCGA2/11_Hayes.pdf [presentation]. The Cancer Genome Atlas 2nd Annual Scientific Symposium; 27–28 Nov 2012; Crystal City, Virginia, US. Accessed 8 January 2015.

41. The Cancer Genome Atlas Research Network (2015) Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature. In press. doi: 10.1038/nature14114 25612050

42. Broad Institute TCGA Genome Data Analysis Center (2013) Mutation Analysis (MutSigCV v0.9). Cambridge (Massachusetts): Broad Institute TCGA Genome Data Analysis Center. doi: 10.7908/C1VH5KV4

43. Cibulskis K, Lawrence MS, Carter SL, Sivachenko A, Jaffe D, et al. (2013) Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotechnol 31: 213–219. doi: 10.1038/nbt.2514 23396013

44. Heagerty PJ, Lumley T, Pepe MS (2000) Time-dependent ROC curves for censored survival data and a diagnostic marker. Biometrics 56: 337–344. 10877287

45. The R Project for Statistical Computing (2015) R [computer program]. Available: http://www.r-project.org. Accessed 8 January 2015.

46. Marur S, Forastiere AA (2008) Head and neck cancer: changing epidemiology, diagnosis, and treatment. Mayo Clin Proc 83: 489–501. doi: 10.4065/83.4.489 18380996

47. Marur S, D’Souza G, Westra WH, Forastiere AA (2010) HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol 11: 781–789. doi: 10.1016/S1470-2045(10)70017-6 20451455

48. Marusyk A, Tabassum DP, Altrock PM, Almendro V, Michor F, et al. (2014) Non-cell-autonomous driving of tumour growth supports sub-clonal heterogeneity. Nature 514: 54–58. doi: 10.1038/nature13556 25079331

49. Mroz EA, Rocco JW (2012) Gene expression analysis as a tool in early-stage oral cancer management. J Clin Oncol 30: 4053–4055. doi: 10.1200/JCO.2012.44.8050 23045572

50. Lindgren D, Hoglund M, Vallon-Christersson J (2011) Genotyping techniques to address diversity in tumors. Adv Cancer Res 112: 151–182. doi: 10.1016/B978-0-12-387688-1.00006-5 21925304